Butlletí de la Institució Catalana d’Història Natural, 78: 119-123. 2014 ISSN 2013-3987 (online edition): ISSN: 1133-6889 (print edition)119 gea, flora et fauna GEA, FLORA ET FAUNA

First record of the invasive tingid species Corythauma ayyari (Drake, 1933) in the Iberian Peninsula (Insecta: : : )

Marcos Roca-Cusachs* & Marta Goula**

* Departament de Biologia . Facultat de Biologia. Universitat de Barcelona (UB). Avda. Diagonal, 643. 08028 Barcelona. A/e: marcosrocacusachs@ gmail.com ** Departament de Biologia Animal and Institut de Recerca de la Biodiversitat (IRBio). Facultat de Biologia. Universitat de Barcelona (UB). Avda. Diagonal, 643. 08028 Barcelona. A/e: [email protected] Corresponding author: Marcos Roca-Cusachs. A/e: [email protected]

Rebut: 18.11.2014; Acceptat: 03.12.2014; Publicat: 29.12.2014

Abstract

Corythauma ayyari (Drake, 1933) (Heteroptera: Tingidae) is reported for the first time in the Iberian Peninsula. Four specimens were collected in Puigmoltó (Sant Pere de Ribes, Barcelona, Spain), 45 km southwest of Barcelona city. This Oriental invasive species may become pest causing necrosis on the leaves of its host plant species, usually ornamental plants, among which jasmine (Jasminum sp.) is the most common. Key words: invasive species, allochtonous species, lace bug, jasmin, pest, Tingidae, Hemiptera, Heteroptera.

Resum

Primera cita per l’espècie invasora Corythauma ayyari (Drake, 1933) a la península Ibèrica (Insecta, Hemiptera, Heteroptera, Tingidae)

Corythauma ayyari (Drake, 1933) (Heteroptera: Tingidae) ha estat trobat per primer cop a la península Ibèrica. Es van recol·lectar quatre individus a la localitat de Puigmoltó (Sant Pere de Ribes, Barcelona) a 45 km al sudoest de la ciutat de Barcelona. Aquesta espècie invasora oriental pot convertir-se en plaga, ocasionant necrosis a les fulles. Amb freqüencia les seves plantes hostes són plantes ornamen- tals, entre les quals el gessamí (Jasminum sp.) és la més comuna. Paraules clau: Espècie invasora, espècie aŀlòctona, tigre del gesamí, gesamí, plaga, Tingidae, Hemiptera, Heteroptera.

Introduction (Coreidae) (Ribes & Escolà, 2005), the plant bugs Deraeo- coris flavilinea (A. Costa, 1862) (Miridae) (Gessé. 2011) and The history of species introductions in Europe is not new, Fulvius borgesi Chérot, J. Ribes & Gorczyca 2006 (Miridae) though the phenomenon has grown faster in the last centu- (Chérot & Pagola-Carte, 2012), the plane tree bug Arocatus ry as a result of increasing globalization, climate change, longiceps Stål, 1872 () (Ribes & Pagola-Carte, the worldwide exchange of goods and tourists affecting the 2008), the sycamore seed bug Belonochilus numenius Say, abundance and dispersion of invasive allochthonous species 1832 (Lygaeidae) (Gessé et al., 2009), the dirt-colored seed and the vulnerability of ecosystems to invasions. Often refer- bug biguttula Stål (Lygaeidae) (Baena & Torres, red to as «aliens» these invasive allochtonous species may 2012), 1874 (Baena & Torres, 2012), the leafhopper assas- have significant environmental, economic and public health sin bug Zelus renardii Kolenati, 1856 (Reduviidae) (Vivas, impact as they represent a significant risk for the wholesale 2012), and the andromeda lace bug takeyai (Dra- homogenization of ecosystems (Genovesi & Shine, 2004). ke & Maa, 1955) (Tingidae) (Pérez-Otero & Mansilla, 2012). About 50 % of recently invading species belong to the He- Taxonomic composition of the allochtonous Heteroptera miptera order. Among true bugs (suborder Heteroptera), from of Europe is mainly built up by Miridae (17 species, 40 %), 2005 onwards the alien species reported in the Iberian Penin- Tingidae (9 species, 21 %), and Anthocoridae (5 species, sula are as follows: the broad-headed bug Heegeria tangirica 12 %), all of which are overrepresented compared to the nati- Saunders, 1877 (Alydiidae) (Burger, 2011), the Western co- ve European Heteroptera fauna. More than half of the species nifer seed bug Leptoglossus occidentalis Heidemann, 1910 are phytophagous (24 species, 57 %) and the advantage of

Butlletí ICHN 78, 2014 120 M. ROCA-CUSACHS & M. GOULA GEA, FLORA ET FAUNA trophic specialization in invasion success was discussed by Rabitsch (2008). The main objective of the present work is to report the first Iberian collection of the jasmine lace bug Corythauma ayya- ri (Drake, 1933). In addition, we summarize its biology and current distribution in the Mediterranean Basin, and aim at facilitating its identification by means of a short description including pictures, and emendations to the identification key of Euromediterranean Tingidae (Péricart, 1983) to include genus Corythauma Drake & Poor, 1939.

Description, biology and distribution of C. ayyari

Corythauma ayyari is a tiny unhairy (♀: 2.46– 2.71 mm; ♂: 2.57– 2.75 mm; Novoselsky & Freidberg 2013; our female specimens: 2.9 mm both; our male specimens: 3.1 mm both). Dorsal general coloration is whitish, with darker areas or stripes scattered on the pronotum, the scutellum and the hemelytra (Fig. 1a, b). Body is brownish, while antennae and legs are light brown colored, darker at the last antennal joint. Bucculae joint anteriorly, hiding labrum in a frontal view (Fig. 1c, d). The most catching-eye feature of C. ayyari is the almost spheric dome in the pronotum, truncate anteri- orly (Fig. 1b). Thus, head is visible from eyes forwards. Also, pronotum presents three very prominent longitudinal cari- nae. Pronotal margins show very tiny, setigerous tubercles, poorly seen even at high magnification (160x). Metasternal scent glands canals are discernible. Sexual dimorphism only concerns the apex of abdomen, as may be seen in figure 1c (female) and figure 1d (male). Left male paramer is sickle shaped with a concave interior margin (Fig. 2). Adults merge at night and are short-lived. Males live up to 10 days while females last up to 12.3 days. Mating occurs at the first day of postemergence and is followed by a 2.7 day preoviposition, 8.2 days of oviposition and 1.7 days of pos- toviposition. The eggs require incubation between 9 and 11 days (Schaefer & Panizzi, 2000). Preliminary observations suggest that this species has overlapping generations and has the potential to establish reproductive colonies in the Medi- terranean Basin (Pedata et al., 2013). Corythauma ayyari has been found in several ornamental plants, a list from different authors being compiled by Pedata et al. (2013): Althea offici- nalis (marshmallow), Daedalacanthus nervosus (blue sage), Figure 1. Habitus of Corythauma ayyari: (a) dorsal view, (b) lateral view, Hedychium sp. (cardamon), Jasminum officinalis, J. sambac (c) female in ventral view, and (d) male in ventral view. Scale: 0.1 mm. (= Jasminum pubescens) (jasmin), Lantana sp. (verbane), Musa sp. (banana), Ocimum sp. (basilicum), Trachelosper- mum sp. (star jasmine) and Volkameria inermis (= Clerodend- et al., 1996; Schaefer & Panizzi, 2000). The leaf undersides rum inerme) (wild jasmine). Although highly polyphagous, become black or dark brown and become spotted as an ef- C. ayyari is to be considered as a pest of jasmin in Southern fect of the excrements and the photosynthesis is reduced as India (Schaefer & Panizzi 2000). However, not all Jasminum a direct effect of the palisade parenchyma damage (Novo- species are infested. For example, Pedata et al. (2013) report selsky & Freidberg, 2013). This ensemble of symptoms may that Jasminum polyanthum, J. multiflorum, J. nudiflorum, J. be easily confused with those caused by other lace bugs. humile and Trachelospermum sp. were unsuccessfully pros- Manual collection of infected leaves may be a successful pected in the vicinity of the J. sambac occupied by C. ayyari. method to manage C. ayyari (Nair & Nair, 1974; Singh & Both adults and nymphs feed on sap from leaves of the host Satyanarayana, 1996). plants. The infected leaves show small yellow chlorate spots Corythauma ayyari is an Oriental tingid bug species that on the upper surface, desiccate and eventually drop (Buntin is found originally in Pakistan (Drake & Man 1964), India,

Butlletí ICHN 78, 2014 FIRST RECORD OF THE CORYTHAUMA AYYARI (DRAKE, 1933) IN THE IBERIAN PENINSULA 121 GEA, FLORA ET FAUNA

Results and discussion

Material studied 2 MM, 2 FF, 27.IX.2014 (M. Roca-Cusachs leg. et det.) and 11 MM, 13 FF on Jasminum grandiflorum 06.XII.2014 (M. Roca-Cusachs leg. et det.) Puigmoltó, Sant Pere de Ri- bes, Barcelona, Spain, +41.2484, -1.7674. The specimens have been dry mounted, four individuals have been donated to the «Centre de Recursos de Biodiversitat Animal» (CRBA Universitat de Barcelona), four to the «Museu de Ciències Naturals de Barcelona» and 16 have been kept in the authors’ personal collections. Specimens were collected in a private 10 square meters backyard (Fig. 4). The backyard is found in Figure 2. Left male paramere of Corythauma ayyari. Scale 0.1 mm. a periurban residential area, next to natural woods and uncul- tivated lands. Cultivated species in the backyard were plan- ted around ten years ago, and belong to Vitis vinifera (grape Laos, Malaysia, Thailand and Singapore (Nair & Nair, 1974; wine), Citrus sp. (lemon tree), Yuca filamentosa, Bougainvi- Guilbert, 2007). C. ayyari has recently been reported from llea sp., Gardenia ssp. and Jasminum grandiflorum. The first France (Streito et al., 2010, samples collected in Puget-sur- four individuals where found in a white wall nearby, while Argens, Var, 12 September 2009), Israel (Novoselsky & the last collections were made on J. grandiflorum, adding this Freidberg, 2013, samples collected in Tel-Aviv area, August- species in the list of host plants of C. ayyari. October 2004-2011) and Italy (Pedata et al., 2013, samples The circumstances of our C. ayyari collections fit those collected in Caserta, Campania, November and December in Italy (a single plant of J. sambac in a balcony) or France 2013), as first records in the Euromediterranean region (Fig. (small green area in a highway resting area). 3). Identification Material and methods Two Palaearctic Tingidae show a spheric pronotal dome: Sphaerista paradoxa (Jakovlev, 1880) and Galeatus scrophi- Samples were collected by hand, preserved in 70% ethanol cus Saunders, 1876. However, in those two species bucculae and identified using a Leica MZ125 binocular microscope. do not joint anteriorly, thus labrum is visible from a frontal Pictures were taken with a Leica DFC450 camera coupled view, and their habitus clearly does not fit with our speci- to a Leica MZ160A binocular microscope using alcoholic mens characteristics. The specimens might also erroneously based hand cleaning gel. The physical properties of this gel be attributed either to Stephanitis pyri (Fabricius, 1775) or provide an ideal medium to manipulate tiny specimens for S. pyrioides (Scott, 1874), but in Stephanitis spp. pronotum photography. The specimens have been dry mounted and are projects all over the head, which is thus invisible from dorsal kept in Roca-Cusachs personal collection. view.

Figure 3. Map of the current Mediterranean distribution of Corythauma ayyari.

Butlletí ICHN 78, 2014 122 M. ROCA-CUSACHS & M. GOULA GEA, FLORA ET FAUNA

Thailand was inspected. In fact, this South France route of entrance has recently been modelled for Drosophyla suzukii (Matsumura, 1931) (Cini et al., 2014). Israelian collections of C. ayyari in Tel-Aviv area also might suggest the role of Tel-Aviv harbor in the introduction of alien species through the Lessepsian trading route (along the Red Sea through the Suez Canal), but further evidences need to be gathered.

Conclusions

In a globalized world, invasions are expected to occur more often and at greater scale than ever. Within the Euro- pean Union-funded Framework Programme, three-years Re- search Project DAISIE (Delivering Alien Invasive Species Inventories for Europe) (2005–2007), an inventory of the Figure 4. View of the backyard where Corythauma ayyari was found alien (non-native, non-indigenous, exotic) species of Europe (Puigmoltó, Sant Pere de Ribes, Barcelona). was completed and made available via the Internet (www. europe-aliens.org). More than 12,122 invading species were reported, and 2,740 were terrestrial invertebrates, which were mainly introduced by transportation associated to horti- Using the key to Euromediterranean Tingidae (Péricart, cultural activities (DAISIE, S. A.). 1983), the collected specimens may be run into Lasiacantha Increasing demand to live in residential areas, and chang- Stål. However, general habitus and much longer and abundant ing trends in the market to cover the demand to have access to pilosity in Lasiacantha clearly show that the specimens do not new, different, until now unknown ornamental plant species belong to it. As C. ayyari is now being reported from different from everywhere in the world, foster intense intercontinental Euromediterranean countries, and Péricart’s work is the most widespread identifying work, we propose an accommodation live plant commerce. As an example, in Spain importation of of that key to include this allochtonous genus, affecting dichot- live plant goods grew 9,17 % comparing the first semester of omic points 23 to 26 (Péricart, 1983. P. 74-75). 2013 with first semester of 2014. However, to trace the ori- gin of imported plants is not easy, as trading may occur with 23 (26) Anterior margin of pronotum swollen. Scent major retailers which in turn provides in further countries all gland canals discernible...... 23a, 23b over the world (Pol López com. pers., Catalan Federation of Plant Nurseries). 23a (23b) Anterior margin of pronotum spherically swol- Thus, chances for species associated to live orna- len and only slightly projecting over the posterior mental plants to expand with international trading are greatly head margin; most of the head, eyes included, is dorsally visible...... Corythauma Stål increasing. However, invasive is not necessarily synonym of noxious (pest) species. The European and Mediterranean 23b (23b) Anterior margin of pronotum otherwise swollen, Plant Protection Organization has already reported C. ayyari and conspicuously projecting forwards, com- in its area of influence (EPPO, 2013), but the species is not in pletely hiding the head ally...... 24 the list of alert or menacing species. Only more observations 24 (25) As in Péricart (1983)...... Corythuca Stål and reports may give the clues for C. ayyari future history 25 (24) As in Péricart (1983) ...... Stephanitis Stål out of its original distribution area. 26 (23) Genera not presenting simultaneously the margin of pronotum swollen and the scent gland canals discernible...... 27 Acknowledgements

Entry way The authors are grateful for the interest shown by the ow- ners of the garden where C. ayyari was found, by means of Some authors state Italy as to be the most common door providing a photograph of the garden and looking for any of entrance to Europe, due to its location in the middle of more evidence of C. ayyari, though no more individuals have the Mediterranean Basin (Jucker et al., 2008). South Fran- been observed until present. Authors are also in debt with ce could be also a very important entry door of alien species Catalan Federation of Plant Nurseries («Federació d’Agri- to Europe, particularly through Marseille, which is the most cultors Viveristes de Catalunya», in the person of Pol López) important Mediterranean harbour. Streito et al. (2010) report for his kind offer of statistical data on live plant importations that an specimen of the also invasive lace bug species Step- hanitis typica (Distant, 1903) was collected in Marseille har- in Spain. bor in September 2009 when a lot of Musa sp. coming from

Butlletí ICHN 78, 2014 FIRST RECORD OF THE CORYTHAUMA AYYARI (DRAKE, 1933) IN THE IBERIAN PENINSULA 123 GEA, FLORA ET FAUNA

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